Conundrum: How do self-infertile plants pass on the trait through random processes

Self-fertilization is a problem, as it leads to inbreeding. Recognition systems that prevent self-fertilization have evolved to ensure that a plant mates only with a genetically different plant and not with itself. The recognition systems underlying self-incompatibility are found all around us in nature, and can be found in at least 100 plant families and 40% of species.

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In plants such as snapdragons and Petunia, when the pollen lands on the stigma, it germinates and starts growing. The stigma, however, contains a toxin (an SRNase) that stops pollen growth. Pollen in turn has a team of genes (F-box genes) that produce antidotes to all toxins except for the toxin produced by the “self” stigma. Therefore, pollen can fertlize when it lands on stigma that does not belong to the same plant, but not when it lands on the plant’s own stigma. It may seem like a harsh system, but plants can use this toxin-antidote system to ensure that they only mate with a genetically different plant. This is important as self-fertilization leads to inbreeding, which is detrimental for the offspring.

It doesn’t seem “harsh,” it seems complex, not what one would expect of truly random evolution.

Non-self recognition systems are found all around us in nature and have an astonishing diversity of mating types, so the big question in their evolution is: how do you evolve a new mating type when doing so requires a mutation in both sides? For example, when there is a change in the female side (stigma), it produces a new toxin for which no other pollen has an antidote — so mating can’t occur. Does this means that there needs to be a change in the male side (pollen) first, so that the antidote appears and then waits for a corresponding change in the stigma (female side)? But how does this co-evolution work when evolution is a random process? Is there a particular order of mutations that is more likely to create a new mating type? Paper. (paywall) – Katarína Boďová, Tadeas Priklopil, David L. Field, Nicholas H. Barton, Melinda Pickup. Evolutionary Pathways for the Generation of New Self-Incompatibility Haplotypes in a Non-self Recognition System. Genetics, 2018; genetics.300748.2018 DOI: 10.1534/genetics.118.300748More.

A friend notes,

The article recognizes a “chicken and egg” paradox, where pollen has antidotes to stigma poisons, so how does a mutation spread?

“For example, when there is a change in the female side (stigma), it produces a new toxin for which no other pollen has an antidote — so mating can’t occur. Does this means that there needs to be a change in the male side (pollen) first, so that the antidote appears and then waits for a corresponding change in the stigma (female side)? But how does this co-evolution work when evolution is a random process?”